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Cadmium interference with iron sensing reveals transcriptional programs sensitive and insensitive to reactive oxygen species
Abstract Iron (Fe) is an essential micronutrient whose uptake is tightly regulated to prevent either deficiency or toxicity. Cadmium (Cd) is a non-essential element that induces both Fe deficiency and toxicity; however, the mechanisms behind these Fe/Cd-induced responses are still elusive. Here we e...
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Published in: | Journal of experimental botany 2022-01, Vol.73 (1), p.324-338 |
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creator | McInturf, Samuel A Khan, Mather A Gokul, Arun Castro-Guerrero, Norma A Höhner, Ricarda Li, Jiamei Marjault, Henri-Baptiste Fichman, Yosef Kunz, Hans-Henning Goggin, Fiona L Keyster, Marshall Nechushtai, Rachel Mittler, Ron Mendoza-Cózatl, David G |
description | Abstract
Iron (Fe) is an essential micronutrient whose uptake is tightly regulated to prevent either deficiency or toxicity. Cadmium (Cd) is a non-essential element that induces both Fe deficiency and toxicity; however, the mechanisms behind these Fe/Cd-induced responses are still elusive. Here we explored Cd- and Fe-associated responses in wild-type Arabidopsis and in a mutant that overaccumulates Fe (opt3-2). Gene expression profiling revealed a large overlap between transcripts induced by Fe deficiency and Cd exposure. Interestingly, the use of opt3-2 allowed us to identify additional gene clusters originally induced by Cd in the wild type but repressed in the opt3-2 background. Based on the high levels of H2O2 found in opt3-2, we propose a model where reactive oxygen species prevent the induction of genes that are induced in the wild type by either Fe deficiency or Cd. Interestingly, a defined cluster of Fe-responsive genes was found to be insensitive to this negative feedback, suggesting that their induction by Cd is more likely to be the result of an impaired Fe sensing. Overall, our data suggest that Fe deficiency responses are governed by multiple inputs and that a hierarchical regulation of Fe homeostasis prevents the induction of specific networks when Fe and H2O2 levels are elevated.
Cadmium induces an iron deficiency response often explained by root uptake competition. Here we show that Cd also impairs Fe sensing in leaves, even when Fe is in sufficient quantities. |
doi_str_mv | 10.1093/jxb/erab393 |
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Iron (Fe) is an essential micronutrient whose uptake is tightly regulated to prevent either deficiency or toxicity. Cadmium (Cd) is a non-essential element that induces both Fe deficiency and toxicity; however, the mechanisms behind these Fe/Cd-induced responses are still elusive. Here we explored Cd- and Fe-associated responses in wild-type Arabidopsis and in a mutant that overaccumulates Fe (opt3-2). Gene expression profiling revealed a large overlap between transcripts induced by Fe deficiency and Cd exposure. Interestingly, the use of opt3-2 allowed us to identify additional gene clusters originally induced by Cd in the wild type but repressed in the opt3-2 background. Based on the high levels of H2O2 found in opt3-2, we propose a model where reactive oxygen species prevent the induction of genes that are induced in the wild type by either Fe deficiency or Cd. Interestingly, a defined cluster of Fe-responsive genes was found to be insensitive to this negative feedback, suggesting that their induction by Cd is more likely to be the result of an impaired Fe sensing. Overall, our data suggest that Fe deficiency responses are governed by multiple inputs and that a hierarchical regulation of Fe homeostasis prevents the induction of specific networks when Fe and H2O2 levels are elevated.
Cadmium induces an iron deficiency response often explained by root uptake competition. Here we show that Cd also impairs Fe sensing in leaves, even when Fe is in sufficient quantities.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/erab393</identifier><identifier>PMID: 34499172</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Cadmium - metabolism ; Cadmium - toxicity ; Gene Expression Regulation, Plant ; Hydrogen Peroxide ; Iron - metabolism ; Plant Roots - metabolism ; Reactive Oxygen Species</subject><ispartof>Journal of experimental botany, 2022-01, Vol.73 (1), p.324-338</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c357t-81bea8c35504d2f34446729fa29855256678f8f907ff83de74c8475534573a2c3</citedby><cites>FETCH-LOGICAL-c357t-81bea8c35504d2f34446729fa29855256678f8f907ff83de74c8475534573a2c3</cites><orcidid>0000-0002-4141-3106 ; 0000-0002-8645-2694 ; 0000-0001-8000-0817 ; 0000-0002-9616-0791</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34499172$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Cuypers, Ann</contributor><creatorcontrib>McInturf, Samuel A</creatorcontrib><creatorcontrib>Khan, Mather A</creatorcontrib><creatorcontrib>Gokul, Arun</creatorcontrib><creatorcontrib>Castro-Guerrero, Norma A</creatorcontrib><creatorcontrib>Höhner, Ricarda</creatorcontrib><creatorcontrib>Li, Jiamei</creatorcontrib><creatorcontrib>Marjault, Henri-Baptiste</creatorcontrib><creatorcontrib>Fichman, Yosef</creatorcontrib><creatorcontrib>Kunz, Hans-Henning</creatorcontrib><creatorcontrib>Goggin, Fiona L</creatorcontrib><creatorcontrib>Keyster, Marshall</creatorcontrib><creatorcontrib>Nechushtai, Rachel</creatorcontrib><creatorcontrib>Mittler, Ron</creatorcontrib><creatorcontrib>Mendoza-Cózatl, David G</creatorcontrib><title>Cadmium interference with iron sensing reveals transcriptional programs sensitive and insensitive to reactive oxygen species</title><title>Journal of experimental botany</title><addtitle>J Exp Bot</addtitle><description>Abstract
Iron (Fe) is an essential micronutrient whose uptake is tightly regulated to prevent either deficiency or toxicity. Cadmium (Cd) is a non-essential element that induces both Fe deficiency and toxicity; however, the mechanisms behind these Fe/Cd-induced responses are still elusive. Here we explored Cd- and Fe-associated responses in wild-type Arabidopsis and in a mutant that overaccumulates Fe (opt3-2). Gene expression profiling revealed a large overlap between transcripts induced by Fe deficiency and Cd exposure. Interestingly, the use of opt3-2 allowed us to identify additional gene clusters originally induced by Cd in the wild type but repressed in the opt3-2 background. Based on the high levels of H2O2 found in opt3-2, we propose a model where reactive oxygen species prevent the induction of genes that are induced in the wild type by either Fe deficiency or Cd. Interestingly, a defined cluster of Fe-responsive genes was found to be insensitive to this negative feedback, suggesting that their induction by Cd is more likely to be the result of an impaired Fe sensing. Overall, our data suggest that Fe deficiency responses are governed by multiple inputs and that a hierarchical regulation of Fe homeostasis prevents the induction of specific networks when Fe and H2O2 levels are elevated.
Cadmium induces an iron deficiency response often explained by root uptake competition. Here we show that Cd also impairs Fe sensing in leaves, even when Fe is in sufficient quantities.</description><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Cadmium - metabolism</subject><subject>Cadmium - toxicity</subject><subject>Gene Expression Regulation, Plant</subject><subject>Hydrogen Peroxide</subject><subject>Iron - metabolism</subject><subject>Plant Roots - metabolism</subject><subject>Reactive Oxygen Species</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp9kM9LwzAUx4Mobk5P3qUnEaQuzY-mOcrwFwy86Llk6cvMaNOatLqBf7zRTb15et8Hn_fh8UXoNMNXGZZ0ulovpuDVgkq6h8YZy3FKGM320RhjQlIsuRihoxBWGGOOOT9EI8qYlJkgY_QxU1VjhyaxrgdvwIPTkLzb_iWxvnVJABesWyYe3kDVIem9ckF72_W2dapOOt8uvWrCFuztGyTKVdH2t_dtvFb6O7frzRKitQNtIRyjAxOlcLKbE_R8e_M0u0_nj3cPs-t5qikXfVpkC1BFzByzipj4PMsFkUYRWXBOeJ6LwhRGYmFMQSsQTBdMcE4ZF1QRTSfoYuuN374OEPqysUFDXSsH7RBKwkWGmWSMRvRyi2rfhuDBlJ23jfKbMsPlV91lrLvc1R3ps514WDRQ_bI__UbgfAu0Q_ev6RMUUovr</recordid><startdate>20220105</startdate><enddate>20220105</enddate><creator>McInturf, Samuel A</creator><creator>Khan, Mather A</creator><creator>Gokul, Arun</creator><creator>Castro-Guerrero, Norma A</creator><creator>Höhner, Ricarda</creator><creator>Li, Jiamei</creator><creator>Marjault, Henri-Baptiste</creator><creator>Fichman, Yosef</creator><creator>Kunz, Hans-Henning</creator><creator>Goggin, Fiona L</creator><creator>Keyster, Marshall</creator><creator>Nechushtai, Rachel</creator><creator>Mittler, Ron</creator><creator>Mendoza-Cózatl, David G</creator><general>Oxford University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-4141-3106</orcidid><orcidid>https://orcid.org/0000-0002-8645-2694</orcidid><orcidid>https://orcid.org/0000-0001-8000-0817</orcidid><orcidid>https://orcid.org/0000-0002-9616-0791</orcidid></search><sort><creationdate>20220105</creationdate><title>Cadmium interference with iron sensing reveals transcriptional programs sensitive and insensitive to reactive oxygen species</title><author>McInturf, Samuel A ; Khan, Mather A ; Gokul, Arun ; Castro-Guerrero, Norma A ; Höhner, Ricarda ; Li, Jiamei ; Marjault, Henri-Baptiste ; Fichman, Yosef ; Kunz, Hans-Henning ; Goggin, Fiona L ; Keyster, Marshall ; Nechushtai, Rachel ; Mittler, Ron ; Mendoza-Cózatl, David G</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c357t-81bea8c35504d2f34446729fa29855256678f8f907ff83de74c8475534573a2c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Cadmium - metabolism</topic><topic>Cadmium - toxicity</topic><topic>Gene Expression Regulation, Plant</topic><topic>Hydrogen Peroxide</topic><topic>Iron - metabolism</topic><topic>Plant Roots - metabolism</topic><topic>Reactive Oxygen Species</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>McInturf, Samuel A</creatorcontrib><creatorcontrib>Khan, Mather A</creatorcontrib><creatorcontrib>Gokul, Arun</creatorcontrib><creatorcontrib>Castro-Guerrero, Norma A</creatorcontrib><creatorcontrib>Höhner, Ricarda</creatorcontrib><creatorcontrib>Li, Jiamei</creatorcontrib><creatorcontrib>Marjault, Henri-Baptiste</creatorcontrib><creatorcontrib>Fichman, Yosef</creatorcontrib><creatorcontrib>Kunz, Hans-Henning</creatorcontrib><creatorcontrib>Goggin, Fiona L</creatorcontrib><creatorcontrib>Keyster, Marshall</creatorcontrib><creatorcontrib>Nechushtai, Rachel</creatorcontrib><creatorcontrib>Mittler, Ron</creatorcontrib><creatorcontrib>Mendoza-Cózatl, David G</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of experimental botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>McInturf, Samuel A</au><au>Khan, Mather A</au><au>Gokul, Arun</au><au>Castro-Guerrero, Norma A</au><au>Höhner, Ricarda</au><au>Li, Jiamei</au><au>Marjault, Henri-Baptiste</au><au>Fichman, Yosef</au><au>Kunz, Hans-Henning</au><au>Goggin, Fiona L</au><au>Keyster, Marshall</au><au>Nechushtai, Rachel</au><au>Mittler, Ron</au><au>Mendoza-Cózatl, David G</au><au>Cuypers, Ann</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cadmium interference with iron sensing reveals transcriptional programs sensitive and insensitive to reactive oxygen species</atitle><jtitle>Journal of experimental botany</jtitle><addtitle>J Exp Bot</addtitle><date>2022-01-05</date><risdate>2022</risdate><volume>73</volume><issue>1</issue><spage>324</spage><epage>338</epage><pages>324-338</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>Abstract
Iron (Fe) is an essential micronutrient whose uptake is tightly regulated to prevent either deficiency or toxicity. Cadmium (Cd) is a non-essential element that induces both Fe deficiency and toxicity; however, the mechanisms behind these Fe/Cd-induced responses are still elusive. Here we explored Cd- and Fe-associated responses in wild-type Arabidopsis and in a mutant that overaccumulates Fe (opt3-2). Gene expression profiling revealed a large overlap between transcripts induced by Fe deficiency and Cd exposure. Interestingly, the use of opt3-2 allowed us to identify additional gene clusters originally induced by Cd in the wild type but repressed in the opt3-2 background. Based on the high levels of H2O2 found in opt3-2, we propose a model where reactive oxygen species prevent the induction of genes that are induced in the wild type by either Fe deficiency or Cd. Interestingly, a defined cluster of Fe-responsive genes was found to be insensitive to this negative feedback, suggesting that their induction by Cd is more likely to be the result of an impaired Fe sensing. Overall, our data suggest that Fe deficiency responses are governed by multiple inputs and that a hierarchical regulation of Fe homeostasis prevents the induction of specific networks when Fe and H2O2 levels are elevated.
Cadmium induces an iron deficiency response often explained by root uptake competition. Here we show that Cd also impairs Fe sensing in leaves, even when Fe is in sufficient quantities.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>34499172</pmid><doi>10.1093/jxb/erab393</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-4141-3106</orcidid><orcidid>https://orcid.org/0000-0002-8645-2694</orcidid><orcidid>https://orcid.org/0000-0001-8000-0817</orcidid><orcidid>https://orcid.org/0000-0002-9616-0791</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Cadmium - metabolism Cadmium - toxicity Gene Expression Regulation, Plant Hydrogen Peroxide Iron - metabolism Plant Roots - metabolism Reactive Oxygen Species |
title | Cadmium interference with iron sensing reveals transcriptional programs sensitive and insensitive to reactive oxygen species |
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